Skip to main content Accessibility help
×
×
Home

Population genetics of multi-host parasites – the case for molecular epidemiological studies of Schistosoma japonicum using larval stages from naturally infected hosts

  • J. SHRIVASTAVA (a1), C. M. GOWER (a1), E. BALOLONG (a2), T. P. WANG (a3), B. Z. QIAN (a4) and J. P. WEBSTER (a1)...
Abstract

Population genetics of multi-host pathogens offers great potential for the understanding of their complex epidemiology but care must be taken to ensure that the sampling procedure does not bias estimates of population indices. The transfer of material to laboratory passage, in particular, runs the risk of bottlenecking and imposing non-random host-induced selection pressures according to the hosts used in passage. We present a novel technique allowing single-locus microsatellite genotyping of the naturally sampled larval stages, enabling unbiased population genetic studies of the multi-host zoonotic parasite Schistosoma japonicum. The utility of these larval genotyping methods for molecular epidemiological studies are illustrated in results from 3 separate data sets. In the first data set, potential loss of alleles based on the definitive host species used for laboratory maintenance was identified by comparing adult worm populations derived from mice and rabbits infected with cercarial populations originating from the same set of snails. In the second data set, bottlenecking was demonstrated by the loss of alleles in adult worms derived within a single generation of laboratory maintenance compared to their parent field-collected cercarial samples. In the final data set, comparison of miracidia and adult worms recovered from naturally infected animals demonstrated that larval analyses can provide stage-specific epidemiological information and that population genetics of schistosomes can be well described by analysis of larval stages. Our results thus advocate the use of natural life-cycle stages to obtain an accurate and ethical representation of the population genetic structure of S. japonicum and other multi-host pathogens.

Copyright
Corresponding author
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Hospital Campus), Norfolk Place, London W2 1PG, UK. Tel: +0207 594 3819. Fax: +0207 402 3927. E-mail: jaya.shrivastava@imperial.ac.uk
References
Hide All

REFERENCES

Barker, G. C. and Bundy, D. A. P. ( 1999). Isolation of a gene family that encodes the porin-like proteins from the human parasitic nematode Trichuris trichuria. Gene 229, 131136.
Bogh, H. O., Zhu, X. Q., Qian, B. Z. and Gasser, R. B. ( 1999). Scanning for nucleotide variations in mitochondrial DNA fragments of Schistosoma japonicum by single-strand conformation polymorphism. Parasitology 118, 7382.
Bowles, J., Hope, M., Tiu, W. U., Liu, X. and McManus, D. P. ( 1993). Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta tropica 55, 217229.
Bergquist, N. R. ( 1995). Controlling schistosomiasis by vaccination: a realistic option? Parasitology Today 11, 191194.
Chen, M. G. and Feng, Z. ( 1999). Schistosomiasis control in China. Parasitology International 48, 1119.
Chen, X. Y., Jiang, Q. W. and Zhao, G. M. ( 2001). Communication of endemic status of schistosomiasis in China in 2000. Chinese Journal of Schistosomiasis Control 13, 129131.
Chilton, N. B., Qian, B. Z., Bogh, H. O. and Nansen, P. ( 1999). An electrophoretic comparison of Schistosoma japonicum (Trematoda) from different provinces in the People's Republic of China suggests the existence of cryptic species. Parasitology 119, 375383.
Davies, C. M., Fairbrother, E. and Webster, J. P. ( 2002). Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 3138.
Dumag, P. U., Gajudo, C. E., Sena, C. Y., Cardenas, E. C. and Fementira, E. B. ( 1981). Epidemiology of animal Schistosomiasis in the Philippines. Philippine Journal of Animal Industry 36, 123.
Duvall, R. H. and DeWitt, W. B. ( 1967). An improved perfusion technique for recovering adult schistosomes from laboratory animals. American Journal of Tropical Medicine and Hygiene 16, 483486.
Fernandez, T. J. Jr, Petilla, T. and Banez, B. ( 1982). An epidemiological study on Schistosoma japonicum in domestic animals in Leyte, Philippines. Southeast Asian Journal for Tropical Medicine and Public Health 13, 575579.
Gandon, S. ( 2004). Evolution of multi-host parasites. Evolution 58, 455469.
Gasser, R. B., Zhen, Q. B., Nansen, P., Johansen, M. V. and Bogh, H. ( 1996). Use of RAPD for the detection of genetic variation in the human blood fluke, Schistosoma japonicum, from mainland China. Molecular and Cellular Probes 10, 353358.
Guo, S. and Thompson, E. ( 1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361372.
Hagan, P. and Gryseels, B. ( 1994). Schistosomiasis research and the European Community. Tropical Geographical Medicine 46, 259268.
Haydon, D. T., Cleaveland, S., Taylor, L. H. and Laurenson, M. K. ( 2002). Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8, 14681473.
He, Y. X., Hu, Y. Q., Yu, Q. F., Ni, C. H., Xue, H. C., Qiu, L. S. and Xie, M. ( 1994). Strain complex of Schistosoma japonicum in the mainland of China. South East Asian Journal of Tropical Medicine and Public Health 25, 232242.
He, Y. X., Salafsky, B. and Ramaswamy, K. ( 2001). Host--parasite relationships of Schistosoma japonicum in mammalian hosts. Trends in Parasitology 17, 320324.
Hurst, M. H. ( 2000). Pathology and course of natural Schistosoma japonicum infection in pigs: results of field study in Hubei province, China. Annals of Tropical Medicine and Parasitology 94, 461477.
Johansen, M. V., Christensen, N. O. and Nansen, P. ( 1997). In vivo labelling of Schistosoma japonicum cercariae with 35S. Journal of Parasitology 83, 956957.
Kumar, S., Tamura, K., Jakobsen, I. B. and Nei, M. ( 2001). MEGA2: Molecular Evolutionary Genetic Analysis Software. Bioinformatics, Arizona State University, Tempe, Arizona, USA.
Lewis, P. O. and Zaykin, D. ( 2001). Genetic Data Analysis: Computer program for the analysis of allelic data. Version 1.0 (d16c). Free program distributed by the authors over the internet from http://lewis.eeb.uconn.edu/lewishome/software.html
LoVerde, P. T., DeWald, J., Minchella, D. J., Bosshardt, S. C. and Damian, R. T. ( 1985). Evidence for host-induced selection in Schistosoma mansoni. Journal of Parasitology 71, 297301.
Merelender, A. M., Woodruff, D. S., Upatham, S., Viyanant, V. and Yuan, H. C. ( 1987). Large genetic distances between Chinese and Philippine Schistosoma japonicum. Parasitology Today 73, 861863.
Rosenberg, N. A., Pritchard, J. K., Weber, J. L., Cann, H. M., Kidd, K. K., Zhivotovsky, L. A. and Feldman, M. W. ( 2002). Genetic structure of human populations. Science 298, 23812385.
Schneider, S., Roesli, D. and Excoffier, L. ( 2000). Arlequin. Genetics and Biometry Laboratory, University of Geneva, Geneva.
Shrivastava, J., Barker, G. C., Johansen, M. V., Xiaonong, Z., Aligui, G. D., McGarvey, S. T. and Webster, J. P. ( 2003). Isolation and characterisation of polymorphic DNA microsatellite markers from Schistosoma japonicum. Molecular Ecology Notes 3, 406408.
Shrivastava, J., Qian, B. Z., McVean, G. and Webster, J. P. ( 2005). An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Molecular Ecology 14, 839849.
Stohler, R. A., Curtis, J. and Minchella, D. J. ( 2004). A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni. International Journal for Parasitology. 34, 595610.
Taylor, L. H., Latham, S. M. and Woolhouse, M. E. J. ( 2001). Risk factors for human disease emergence. Philosophical Transactions of The Royal Society, London, Series B-Biological Sciences 356, 983989.
Theron, A. and Pointier, J. P. ( 1995). Ecology, dynamics, genetics and divergence of trematode populations in heterogeneous environments: the model of Schistosoma mansoni in the insular focus of Guadeloupe. Research and Reviews in Parasitology 55, 4964.
Theron, A., Sire, C., Rognon, A., Prugnolle, F. and Durnad, P. ( 2004). Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129, 571585.
WORLD HEALTH ORGANIZATION ( 1980). Epidemiology and Control of Schistosomiasis. WHO Technical Report Series No. 643. WHO, Geneva.
Wolfensohn, S. and Lloyd, M. ( 1998). The ethics of using animals in experiments. In Handbook of Laboratory Animal Management and Welfare (2nd Edn), pp. 17, Blackwell Science, Oxford, UK.
Woolhouse, M. E., Taylor, L. H. and Haydon, D. T. ( 2001). Population biology of multihost pathogens. Science 292, 11091112.
Yang, W. P., Goa, F. H., Zhang, C., Yin, N. W. and Xie, J. F. ( 2004). An analysis of epidemic situation on schistosomiasis during the period of 1996 to 2003 in Anhui Province. Chinese Journal of Parasitic Diseases Control 17, 149150.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed